vol. 190, no. 5 the american naturalist november 2017 Toward a Periodic Table of Niches, or Exploring the Lizard Niche Hypervolume Eric R. Pianka,1,* Laurie J. Vitt,2 Nicolás Pelegrin,3 Daniel B. Fitzgerald,4 and Kirk O. Winemiller4 1. Department of Integrative Biology, University of Texas, Austin, Texas 78712; 2. Sam Noble Museum and Department of Biology, University of Oklahoma, Norman, Oklahoma 73072; 3. Laboratorio de Ecología y Conservación de la Herpetofauna, Instituto de Diversidad y Ecología Animal (Consejo Nacional de Investigaciones Científicas y Técnicas–Universidad Nacional de Córdoba [UNC]); and Centro de Zoología Aplicada (UNC), Rondeau 798 X5000AVP Córdoba, Argentina; 4. Program in Ecology and Evolutionary Biology and Department of Wildlife and Fisheries Sciences, Texas A&M University, College Station, Texas 77843 Submitted September 2, 2016; Accepted May 5, 2017; Electronically published August 29, 2017 Online enhancements: appendix, supplementary material. Dryad data: http://dx.doi.org/10.5061/dryad.db901. abstract: Widespread niche convergence suggests that species can Dedication be organized according to functional trait combinations to create a framework analogous to a periodic table. We compiled ecological data I predict there will be erected a two or three way clas- for lizards to examine patterns of global and regional niche diversifi- sification of organisms and their geometrical and tem- cation, and we used multivariate statistical approaches to develop the poral environments, this classification consuming most beginnings for a periodic table of niches. Data (501 variables) for five of the creative energy of ecologists. The future princi- major niche dimensions (habitat, diet, life history, metabolism, de- ples of the ecology of coexistence will then be of the fense) were compiled for 134 species of lizards representing 24 of the 38 extant families. Principal coordinates analyses were performed on form for organisms of type A, in environments of struc- niche dimensional data sets, and species scores for the first three axes ture B, such and such relationships will hold. (Mac- were used as input for a principal components analysis to ordinate spe- Arthur 1972) cies in continuous niche space and for a regression tree analysis to sep- arate species into discrete niche categories. Three-dimensional models facilitate exploration of species positions in relation to major gradients Introduction within the niche hypervolume. The first gradient loads on body size, The niche, a central concept in ecology, describes not only foraging mode, and clutch size. The second was influenced by me- tabolism and terrestrial versus arboreal microhabitat. The third was the environmental conditions required for survival and pos- influenced by activity time, life history, and diet. Natural dichotomies itive fitness but also the organism’s potential impact on its are activity time, foraging mode, parity mode, and habitat. Regres- environment. The niche concept has had a long and some- sion tree analysis identified 103 cases of extreme niche conservatism times controversial history in ecology (Chase and Leibold within clades and 100 convergences between clades. Extending this 2003; Colwell and Rangel 2009). Some ecologists even have approach to other taxa should lead to a wider understanding of niche argued against use of the term because the word has been evolution. used in so many different ways (Margalef 1968; Williamson Keywords: evolutionary convergence, lizard ecology, niche diversifica- 1972). The first ecologist to use the word was Grinnell (1917), tion, niche dimensionality, niche hypervolume, clade niche breadth and for whom the niche included everything that affected the overlap. existence of a species at a given location, including abiotic factors (temperature, rainfall,geomorphology,nestsites,and shelter) as well as biotic factors (food, competitors, mutual- ists, parasites, predators, and potential mates). Later, Grin- nell (1928) linked the niche to the concept of ecological equiv- alents, convergent species with similar ecologies found in different geographic regions. * Corresponding author; e-mail: [email protected]. Elton (1927, p. 64) defined the niche as “the animal’s place ORCIDs: Pianka, http://orcid.org/0000-0003-3915-6945; Pelegrin, http:// in its community, its relations to food and enemies.” Elton orcid.org/0000-0003-0546-3955; Fitzgerald, http://orcid.org/0000-0002-3254-7428; Winemiller, http://orcid.org/0000-0003-0236-5129. imagined a behavioral niche, comparing a species’ niche to “ ‘ ’ – q its profession: When an ecologist says there goes a badger Am. Nat. 2017. Vol. 190, pp. 601 616. 2017 by The University of Chicago. fi 0003-0147/2017/19005-57232$15.00. All rights reserved. he should include in his thoughts some de nite idea of the ani- DOI: 10.1086/693781 mal’s place in the community to which it belongs, just as if This content downloaded from 129.116.079.252 on October 23, 2017 07:06:08 AM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). 602 The American Naturalist he had said ‘there goes the vicar’.” Elton’s functional niche is proposed by Winemiller et al. (2015) that use multivariate essentially a measure of a population’s phenotype. statistics for species ordination within niche space and spe- Perhaps the most influential treatment of the niche con- cies classification based on components of niche dimensional cept was that of Hutchinson (1957), who proposed a hypervol- sets. ume definition encompassing all environmental conditions Of the 10,272 extant reptile species (birds excluded), under which a given target species has positive population 9,905 (96.4%) are squamates. Snakes are represented by growth. Hutchinson distinguished a fundamental niche—rep- 3,576 species (34.7% of reptiles) and amphisbaenians by resenting the potential space occupied in the absence of neg- 193 species (1.9% of reptiles). Although some lizards (such ative effects from other species—from a narrower realized as the pygopodid Lialis) are ecological analogs of snakes, niche when such effects are present. In accordance with this we could not include snakes or amphisbaenians because com- Hutchinsonian concept, niches have often been modeled plete data for all variables and niche dimensions required for as series of bell-shaped resource utilization curves, each cor- this study are lacking. The remaining squamates are referred responding to a particular resource or niche dimension to as lizards, even though both snakes (Serpentes) and am- (MacArthur and Levins 1967; MacArthur 1970; Pianka 1976; phisbaenians (Amphisbaenia) are nested among the cur- Schoener 1977). rently recognized 38 lizard families (Uetz 2016b). Lizards Regardless of which concept is adopted, niches are multi- are currently estimated to comprise 63.4% of all reptiles and dimensional and dynamic, responding to temporal and spa- clearly are among the most taxonomically and ecologically tial variation in abiotic conditions, resources, and competi- diverse groups of tetrapod vertebrates. Except in very cold tor and predator populations, among other things (Hutchinson regions, lizards occur virtually anywhere that still contains 1957; Pianka 1976; Schoener 1977; Chase and Leibold 2003; relatively undisturbed natural habitats, and a few species Colwell and Rangel 2009; Holt 2009; Goodyear and Pianka even persist in degraded areas. Similar to other ectotherms, 2011). This complexity poses a great challenge to empirical lizards obtain their body heat solely from the external en- efforts to describe and compare ecological niches. Neverthe- vironment, as opposed to endotherms (such as birds and less, the multitude of known or suspected convergences in mammals) that produce their own heat internally by means many taxa across the globe suggests that construction of a of oxidative metabolism. Moreover, along with other ecto- niche scheme—a framework analogous to chemistry’s pe- therms such as insects, lizards are low-energy animals (Pough riodic table of elements—might be possible (Pianka 1974). 1980). Bennett and Nagy (1977, p. 700) underscore the great Countering criticism of the idea of periodic tables in ecol- “economy of the saurian mode of life” by pointing out that ogy (Steffen 1996), Winemiller et al. (2015) argued that ecol- “one day’s food supply for a small bird will last a lizard of ogists, natural resource managers, and conservationists al- the same body size more than a month.” Ectothermy has ready use a variety of methods that rely on functional traits distinct advantages over endothermy under harsh and un- and niche classification criteria, and therefore, standardized predictable conditions (Schall and Pianka 1978); by means methods for creating niche frameworks need to be explored. of this thermal tactic, lizards can conserve water and energy They proposed an approach that uses functional trait data by becoming inactive during the heat of midday, during re- organized according to five fundamental niche dimensions source shortages, or whenever difficult physical conditions to produce two types of niche classification schemes: one that occur (such as during heat waves or droughts). Endotherms facilitates analysis of species relationships within the multi- must endure these inhospitable periods at a substantially variate niche space (continuous periodic tables) and one that higher metabolic cost or migrate to more hospitable regions. classifies species into niche categories (discrete periodic ta- Ectothermy